Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Self-assembly of aramid amphiphiles into ultra-stable nanoribbons and aligned nanoribbon threads

Nature Nanotechnology volume 16, pages 447–454 (2021)Cite this article

Subjects

Abstract

Small-molecule self-assembly is an established route for producing high-surface-area nanostructures with readily customizable chemistries and precise molecular organization. However, these structures are fragile, exhibiting molecular exchange, migration and rearrangement—among other dynamic instabilities—and are prone to dissociation upon drying. Here we show a small-molecule platform, the aramid amphiphile, that overcomes these dynamic instabilities by incorporating a Kevlar-inspired domain into the molecular structure. Strong, anisotropic interactions between aramid amphiphiles suppress molecular exchange and elicit spontaneous self-assembly in water to form nanoribbons with lengths of up to 20 micrometres. Individual nanoribbons have a Young’s modulus of 1.7 GPa and tensile strength of 1.9 GPa. We exploit this stability to extend small-molecule self-assembly to hierarchically ordered macroscopic materials outside of solvated environments. Through an aqueous shear alignment process, we organize aramid amphiphile nanoribbons into arbitrarily long, flexible threads that support 200 times their weight when dried. Tensile tests of the dry threads provide a benchmark for Young’s moduli (between ~400 and 600 MPa) and extensibilities (between ~0.6 and 1.1%) that depend on the counterion chemistry. This bottom-up approach to macroscopic materials could benefit solid-state applications historically inaccessible by self-assembled nanomaterials.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Kevlar-inspired AAs self-assemble into ultra-stable nanoribbons capable of hierarchical ordering to form dry macroscopic threads.
Fig. 2: AA nanoribbons exhibit minimal molecular exchange.
Fig. 3: AA nanoribbons have a Young’s modulus of E = 1.7 GPa and a tensile strength of σ* = 1.9 GPa.
Fig. 4: AA nanoribbons are aligned by shear forces and dried to form flexible threads.
Fig. 5: X-ray scattering of solid-state nanoribbon threads demonstrates organized molecular packing, extended hydrogen bonding networks and long-range hierarchical order.

Similar content being viewed by others

Data availability

The data generated and analysed during this study are available from the corresponding author on reasonable request.

References

  1. Whitesides, G. M., Mathias, J. P. & Seto, C. T. Molecular self-assembly and nanochemistry: a chemical strategy for the synthesis of nanostructures. Science 254, 1312–1319 (1991).

    Article  CAS  Google Scholar 

  2. Aida, T., Meijer, E. & Stupp, S. I. Functional supramolecular polymers. Science 335, 813–817 (2012).

    Article  CAS  Google Scholar 

  3. Zhang, S. et al. A self-assembly pathway to aligned monodomain gels. Nat. Mater. 9, 594–601 (2010).

    Article  CAS  Google Scholar 

  4. Koutsopoulos, S., Unsworth, L. D., Nagai, Y. & Zhang, S. Controlled release of functional proteins through designer self-assembling peptide nanofiber hydrogel scaffold. Proc. Natl Acad. Sci. USA 106, 4623–4628 (2009).

    Article  CAS  Google Scholar 

  5. Tantakitti, F. et al. Energy landscapes and functions of supramolecular systems. Nat. Mater. 15, 469–476 (2016).

    Article  CAS  Google Scholar 

  6. Ortony, J. H. et al. Internal dynamics of a supramolecular nanofibre. Nat. Mater. 13, 812–816 (2014).

    Article  CAS  Google Scholar 

  7. Schief, W., Touryan, L., Hall, S. & Vogel, V. Nanoscale topographic instabilities of a phospholipid monolayer. J. Phys. Chem. B 104, 7388–7393 (2000).

    Article  CAS  Google Scholar 

  8. da Silva, R. M. et al. Super-resolution microscopy reveals structural diversity in molecular exchange among peptide amphiphile nanofibres. Nat. Commun. 7, 11561 (2016).

    Article  Google Scholar 

  9. Wimley, W. C. & Thompson, T. E. Transbilayer and interbilayer phospholipid exchange in dimyristoylphosphatidylcholine/dimyristoylphosphatidylethanolamine large unilamellar vesicles. Biochemistry 30, 1702–1709 (1991).

    Article  CAS  Google Scholar 

  10. Ortony, J. H. et al. Water dynamics from the surface to the interior of a supramolecular nanostructure. J. Am. Chem. Soc. 139, 8915–8921 (2017).

    Article  CAS  Google Scholar 

  11. Yuan, D., Shi, J., Du, X., Zhou, N. & Xu, B. Supramolecular glycosylation accelerates proteolytic degradation of peptide nanofibrils. J. Am. Chem. Soc. 137, 10092–10095 (2015).

    Article  CAS  Google Scholar 

  12. Toledano, S., Williams, R. J., Jayawarna, V. & Ulijn, R. V. Enzyme-triggered self-assembly of peptide hydrogels via reversed hydrolysis. J. Am. Chem. Soc. 128, 1070–1071 (2006).

    Article  CAS  Google Scholar 

  13. Freeman, R. et al. Reversible self-assembly of superstructured networks. Science 362, 808–813 (2018).

    Article  CAS  Google Scholar 

  14. Williams, R. J. et al. Enzyme-assisted self-assembly under thermodynamic control. Nat. Nanotechnol. 4, 19–24 (2009).

    Article  CAS  Google Scholar 

  15. Hashim, P., Bergueiro, J., Meijer, E. & Aida, T. Supramolecular polymerization: a conceptual expansion for innovative materials. Prog. Polym. Sci. 105, 101250 (2020).

    Article  CAS  Google Scholar 

  16. Xu, Y. et al. Nanostructured polymer films with metal-like thermal conductivity. Nat. Commun. 10, 1771 (2019).

    Article  Google Scholar 

  17. Tuller, H. L. Ionic conduction in nanocrystalline materials. Solid State Ion. 131, 143–157 (2000).

    Article  CAS  Google Scholar 

  18. Sherrington, D. C. & Taskinen, K. A. Self-assembly in synthetic macromolecular systems via multiple hydrogen bonding interactions. Chem. Soc. Rev. 30, 83–93 (2001).

    Article  CAS  Google Scholar 

  19. Dobb, M., Johnson, D. & Saville, B. Supramolecular structure of a high-modulus polyaromatic fiber (Kevlar 49). J. Polym. Sci. Polym. Phys. Ed. 15, 2201–2211 (1977).

    Article  CAS  Google Scholar 

  20. Seyler, H., Storz, C., Abbel, R. & Kilbinger, A. F. A facile synthesis of aramide–peptide amphiphiles. Soft Matter 5, 2543–2545 (2009).

    CAS  Google Scholar 

  21. Claussen, R. C., Rabatic, B. M. & Stupp, S. I. Aqueous self-assembly of unsymmetric peptide bolaamphiphiles into nanofibers with hydrophilic cores and surfaces. J. Am. Chem. Soc. 125, 12680–12681 (2003).

    Article  CAS  Google Scholar 

  22. Yang, M. et al. Dispersions of aramid nanofibers: a new nanoscale building block. ACS Nano 5, 6945–6954 (2011).

    Article  CAS  Google Scholar 

  23. Schleuss, T. W. et al. Hockey-puck micelles from oligo(p-benzamide)-b-PEG rod–coil block copolymers. Angew. Chem. Int. Ed. 45, 2969–2975 (2006).

    Article  CAS  Google Scholar 

  24. Bohle, A. et al. Hydrogen-bonded aggregates of oligoaramide−poly(ethylene glycol) block copolymers. Macromolecules 43, 4978–4985 (2010).

    Article  CAS  Google Scholar 

  25. Abbel, R., Schleuss, T. W., Frey, H. & Kilbinger, A. F. M. Rod-length dependent aggregation in a series of oligo(p-benzamide)-block-poly(ethylene glycol) rod-coil copolymers. Macromol. Chem. Phys. 206, 2067–2074 (2005).

    Article  CAS  Google Scholar 

  26. Johansson, A., Kollman, P., Rothenberg, S. & McKelvey, J. Hydrogen bonding ability of the amide group. J. Am. Chem. Soc. 96, 3794–3800 (1974).

    Article  CAS  Google Scholar 

  27. Dixon, D. A., Dobbs, K. D. & Valentini, J. J. Amide-water and amide-amide hydrogen bond strengths. J. Phys. Chem. 98, 13435–13439 (1994).

    Article  CAS  Google Scholar 

  28. Kline, S. R. Reduction and analysis of SANS and USANS data using IGOR Pro. J. Appl. Crystallogr. 39, 895–900 (2006).

    Article  CAS  Google Scholar 

  29. Nallet, F., Laversanne, R. & Roux, D. Modelling X-ray or neutron scattering spectra of lyotropic lamellar phases: interplay between form and structure factors. J. Phys. II 3, 487–502 (1993).

    CAS  Google Scholar 

  30. Mertens, H. D. & Svergun, D. I. Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J. Struct. Biol. 172, 128–141 (2010).

    Article  CAS  Google Scholar 

  31. Yokoi, H., Kinoshita, T. & Zhang, S. Dynamic reassembly of peptide RADA16 nanofiber scaffold. Proc. Natl Acad. Sci. USA 102, 8414–8419 (2005).

    Article  CAS  Google Scholar 

  32. Hartgerink, J. D., Beniash, E. & Stupp, S. I. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science 294, 1684–1688 (2001).

    Article  CAS  Google Scholar 

  33. Cravotto, G. & Cintas, P. Molecular self-assembly and patterning induced by sound waves. The case of gelation. Chem. Soc. Rev. 38, 2684–2697 (2009).

    Article  CAS  Google Scholar 

  34. Gorelik, T. E., van de Streek, J., Kilbinger, A. F., Brunklaus, G. & Kolb, U. Ab-initio crystal structure analysis and refinement approaches of oligo p-benzamides based on electron diffraction data. Acta Crystallogr. B Struct. Sci. 68, 171–181 (2012).

    Article  CAS  Google Scholar 

  35. Gorelik, T. et al. H-bonding schemes of di- and tri-p-benzamides assessed by a combination of electron diffraction, X-ray powder diffraction and solid-state NMR. CrystEngComm 12, 1824–1832 (2010).

    Article  CAS  Google Scholar 

  36. Wang, J., Liu, K., Xing, R. & Yan, X. Peptide self-assembly: thermodynamics and kinetics. Chem. Soc. Rev. 45, 5589–5604 (2016).

    Article  CAS  Google Scholar 

  37. Barth, A. Infrared spectroscopy of proteins. Biochim. Biophys. Acta Bioenerg. 1767, 1073–1101 (2007).

    Article  CAS  Google Scholar 

  38. Zandomeneghi, G., Krebs, M. R., McCammon, M. G. & Fändrich, M. FTIR reveals structural differences between native β‐sheet proteins and amyloid fibrils. Protein Sci. 13, 3314–3321 (2004).

    Article  CAS  Google Scholar 

  39. Matayoshi, E. D., Wang, G. T., Krafft, G. A. & Erickson, J. Novel fluorogenic substrates for assaying retroviral proteases by resonance energy transfer. Science 247, 954–958 (1990).

    Article  CAS  Google Scholar 

  40. Wu, B., Heidelberg, A. & Boland, J. J. Mechanical properties of ultrahigh-strength gold nanowires. Nat. Mater. 4, 525–529 (2005).

    Article  CAS  Google Scholar 

  41. Smith, J. F., Knowles, T. P., Dobson, C. M., MacPhee, C. E. & Welland, M. E. Characterization of the nanoscale properties of individual amyloid fibrils. Proc. Natl Acad. Sci. USA 103, 15806–15811 (2006).

    Article  CAS  Google Scholar 

  42. Knowles, T. P. et al. Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318, 1900–1903 (2007).

    Article  CAS  Google Scholar 

  43. Lamour, G., Kirkegaard, J. B., Li, H., Knowles, T. P. & Gsponer, J. Easyworm: an open-source software tool to determine the mechanical properties of worm-like chains. Source Code Biol. Med. 9, 16 (2014).

    Article  Google Scholar 

  44. Huang, Y. Y., Knowles, T. P. & Terentjev, E. M. Strength of nanotubes, filaments, and nanowires from sonication‐induced scission. Adv. Mater. 21, 3945–3948 (2009).

    Article  CAS  Google Scholar 

  45. Nassar, R., Wong, E., Gsponer, J. & Lamour, G. Inverse correlation between amyloid stiffness and size. J. Am. Chem. Soc. 141, 58–61 (2019).

    Article  CAS  Google Scholar 

  46. Peng, Z. et al. High tensile strength of engineered β-solenoid fibrils via sonication and pulling. Biophys. J. 113, 1945–1955 (2017).

    Article  CAS  Google Scholar 

  47. Santos, H. M., Lodeiro, C. & Capelo-Martínez, J.-L. in Ultrasound in Chemistry: Analytical Applications 1–16 (Wiley Online Library, 2009).

  48. Lamour, G. et al. Mapping the broad structural and mechanical properties of amyloid fibrils. Biophys. J. 112, 584–594 (2017).

    Article  CAS  Google Scholar 

  49. Zhao, X. et al. Molecular self-assembly and applications of designer peptide amphiphiles. Chem. Soc. Rev. 39, 3480–3498 (2010).

    Article  CAS  Google Scholar 

  50. Niece, K. L., Hartgerink, J. D., Donners, J. J. & Stupp, S. I. Self-assembly combining two bioactive peptide-amphiphile molecules into nanofibers by electrostatic attraction. J. Am. Chem. Soc. 125, 7146–7147 (2003).

    Article  CAS  Google Scholar 

  51. Angeloni, N. L. et al. Regeneration of the cavernous nerve by Sonic hedgehog using aligned peptide amphiphile nanofibers. Biomaterials 32, 1091–1101 (2011).

    Article  CAS  Google Scholar 

  52. Fink, L., Steiner, A., Szekely, O., Szekely, P. & Raviv, U. Structure and interactions between charged lipid membranes in the presence of multivalent ions. Langmuir 35, 9694–9703 (2019).

    Article  CAS  Google Scholar 

  53. Knowles, T. P. & Buehler, M. J. Nanomechanics of functional and pathological amyloid materials. Nat. Nanotechnol. 6, 469–479 (2011).

    Article  CAS  Google Scholar 

  54. Bradbury, R. & Nagao, M. Effect of charge on the mechanical properties of surfactant bilayers. Soft Matter 12, 9383–9390 (2016).

    Article  CAS  Google Scholar 

  55. Takahashi, Y., Ozaki, Y., Takase, M. & Krigbaum, W. Crystal structure of poly(p‐benzamide). J. Polym. Sci. B Polym. Phys. 31, 1135–1143 (1993).

    Article  CAS  Google Scholar 

  56. Paramonov, S. E., Jun, H.-W. & Hartgerink, J. D. Self-assembly of peptide−amphiphile nanofibers: the roles of hydrogen bonding and amphiphilic packing. J. Am. Chem. Soc. 128, 7291–7298 (2006).

    Article  CAS  Google Scholar 

  57. Russell, P. Photonic crystal fibers. Science 299, 358–362 (2003).

    Article  CAS  Google Scholar 

  58. Lindemann, W. R., Christoff-Tempesta, T. & Ortony, J. H. A global minimization toolkit for batch-fitting and χ2 cluster analysis of CW-EPR spectra. Biophys. J. 119, 1937–1945 (2020).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank E. Deiss-Yehiely and C. Settens for their helpful input. We thank R. Allen and L. Hopkins for contributing graphics shown in the figures. We acknowledge J. Tian and S. Kallakuri for contributions to synthesis of early stage AAs that led to the molecular designs incorporated in this report. This material is based upon work supported by the National Science Foundation under grant no. CHE-1945500. This work was supported in part by the Professor Amar G. Bose Research Grant Program, the Abdul Latif Jameel Water and Food Systems Lab, and the MIT Center for Environmental Health Sciences under NIH Center grant P30-ES002109. D.-Y.K. acknowledges the support of the National Research Foundation of Korea’s Basic Science Research Program and Chonbuk National University Fellowship Program. T.C.-T. and W.R.L. acknowledge the support of the National Science Foundation Graduate Research Fellowship Program under grant no. 1122374. T.C.-T. acknowledges the support of the Martin Family Society of Fellows for Sustainability. G.L. acknowledges support from the Université d’Evry-Paris Saclay. This work made use of the MRSEC Shared Experimental Facilities at MIT supported by the National Science Foundation under award number DMR-14-19807 and the MIT Department of Chemistry Instrumentation Facility. X-ray scattering measurements were performed at beamline 12-ID-B of the Advanced Photon Source, a US Department of Energy Office of Science User Facility operated for the US Department of Energy Office of Science by Argonne National Laboratory under contract no. DE-AC02-06CH11357. This work was performed in part at the Harvard University Center for Nanoscale Systems cryo-TEM facility, a member of the National Nanotechnology Coordinated Infrastructure Network, which is supported by the National Science Foundation under award no. 1541959.

Author information

Author notes

  1. Dae-Yoon Kim

    Present address: Institute of Advanced Composite Materials, Korea Institute of Science and Technology, Bondong, Korea

Authors and Affiliations

  1. Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA

    Ty Christoff-Tempesta, Yukio Cho, Dae-Yoon Kim, Michela Geri, William R. Lindemann & Julia H. Ortony

  2. LAMBE, Université Paris-Saclay, University of Evry, CNRS, Evry-Courcouronnes, France

    Guillaume Lamour

  3. Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA, USA

    Andrew J. Lew

  4. X-ray Science Division, Advanced Photon Source, Argonne National Laboratory, Argonne, IL, USA

    Xiaobing Zuo

Authors
  1. Ty Christoff-Tempesta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yukio Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dae-Yoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michela Geri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guillaume Lamour
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andrew J. Lew
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaobing Zuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. William R. Lindemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Julia H. Ortony
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.C.-T., D.-Y. K. and J.H.O. conceived and designed the experiments. D.-Y.K. and T.C.-T. synthesized materials with assistance from W.R.L. and A.J.L.; T.C.-T. and D.-Y.K. performed chemical characterization of all samples. T.C.-T. performed conventional TEM and cryo-TEM. Y.C. and T.C.-T. performed SEM. G.L. performed AFM and statistical topographical analyses. G.L. performed sonication-induced scission measurements, imaging with AFM and TEM, and analysis of data. A.J.L. performed FRET measurements and analysis of the data. X.Z., T.C.-T. and Y.C. performed solution X-ray scattering and analysis of the data. A.J.L. and Y.C. conceptualized nanoribbon thread processing, and Y.C. and M.G. prepared nanoribbon threads. M.G. performed tensile testing of nanoribbon threads and analysis of the data. T.C.-T. and Y.C. performed X-ray scattering of solid-state nanoribbon threads and analysis of the data. J.H.O., T.C.-T and Y.C. cowrote the manuscript. J.H.O. provided project administration, funding acquisition and supervision. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Julia H. Ortony.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Nanotechnology thanks the anonymous reviewers for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–37, Schemes 1–5 and Sections 1–3.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Christoff-Tempesta, T., Cho, Y., Kim, DY. et al. Self-assembly of aramid amphiphiles into ultra-stable nanoribbons and aligned nanoribbon threads. Nat. Nanotechnol. 16, 447–454 (2021). https://doi.org/10.1038/s41565-020-00840-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41565-020-00840-w

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing